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      Risk factors for relapse or persistence of bacteraemia caused by Enterobacter spp.: a case–control study

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          Abstract

          Background

          Enterobacter spp. possess chromosomal AmpC beta-lactamases that may be expressed at high levels. Previous studies have demonstrated a risk of relapsed bacteraemia following therapy with third generation cephalosporins (3GCs). What additional factors predict microbiological failure in Enterobacter bacteraemia is unclear. We aimed to determine factors associated with microbiological failure in Enterobacter bacteraemia.

          Methods

          We retrospectively identified cases of bacteraemia caused by Enterobacter spp. occurring in four hospitals. Using a case–control design, we determined clinical risk factors for persistence or relapse defined as repeated positive blood cultures collected between 72 hours and up to 28 days post initial positive blood culture.

          Results

          During the study period a total of 922 bacteraemia events caused by Enterobacter spp. in adults were identified. The overall risk of relapsed or persisting bacteraemia at 28 days was low (31 of 922, 3.4%), with only 2 patients experiencing emergent resistance to 3GCs. A total of 159 patients were included in the case–control study. Using multivariate logistic regression, independent predictors for relapse were a line-associated source of infection (OR 3.87; 95% CI 1.56-9.60, p = 0.004) and the presence of immunosuppression (OR 2.70; 95% CI 1.14-6.44, p = 0.02). On univariate analysis definitive therapy with a broad-spectrum beta-lactam-beta-lactamase inhibitor (BLBLI, e.g. piperacillin-tazobactam) was not associated with relapse (OR 1.83; 95% CI 0.64-5.21, p = 0.26) although the proportion of patients receiving a BLBLI as definitive therapy was relatively small (21/159, 13.2%).

          Conclusions

          The risk of relapsed or persistent Enterobacter bacteraemia appears to be low in Australia. A line-associated source of infection and immunocompromise were significant independent predictors for relapse. Larger, preferably randomized, studies are needed to address whether BLBLIs represent an effective carbapenem-sparing option for Enterobacter bacteraemia.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13756-017-0177-0) contains supplementary material, which is available to authorized users.

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          Most cited references21

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          Enterobacter spp.: pathogens poised to flourish at the turn of the century.

          W Sanders, C Sanders (1997)
          Knowledge of the genus Enterobacter and its role in human disease has expanded exponentially in recent years. The incidence of infection in the hospital and the community has increased. New clinical syndromes have been recognized. Enterobacter spp. have also been implicated as causes of other syndromes that traditionally have been associated almost exclusively with more easily treatable pathogens, such as group A streptococci and staphylococci. Rapid emergence of multiple-drug resistance has been documented in individual patients during therapy and in populations and environments with strong selective pressure from antimicrobial agents, especially the cephalosporins. Therapeutic options for patients infected with multiply resistant strains have become severely limited. Carbapenems or, alternatively, fluoroquinolones are the most predictively active options, although resistance to both classes has been observed on rare occasions. Enterobacter spp. appear well adapted for survival and even proliferation as the turn of the century approaches.
          Article 0 comments Cited 118 times – based on 0 reviews     Review now
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            Emergence of antibiotic resistance during therapy for infections caused by Enterobacteriaceae producing AmpC beta-lactamase: implications for antibiotic use.

            Seong-Woo Choi, Jie-Oh Lee, Yun-Mi Kim … (2008)
            Enterobacter spp., Serratia marcescens, Citrobacter freundii, and Morganella morganii are characterized by chromosomally encoded AmpC beta-lactamases and possess the ability to develop resistance upon exposure to broad-spectrum cephalosporins. To determine the incidences of the emergence of resistance during antimicrobial therapy for infections caused by these organisms and the effect of the emergence of resistance on patient outcomes, all patients who were admitted to the Asan Medical Center (Seoul, Republic of Korea) from January 2005 to June 2006 and whose clinical specimens yielded Enterobacter spp., S. marcescens, C. freundii, or M. morganii were monitored prospectively. The main end point was the emergence of resistance during antimicrobial therapy. A total of 732 patients with infections were included for analysis. The overall incidence of the emergence of antimicrobial resistance during antimicrobial therapy was 1.9% (14/732). Resistance to broad-spectrum cephalosporins, cefepime, extended-spectrum penicillin, carbapenem, fluoroquinolones, and aminoglycosides emerged during treatment in 5.0% (11/218), 0% (0/20), 2.0% (2/100), 0% (0/226), 0% (0/153), and 1.1% (1/89) of patients, respectively. The emergence of resistance to broad-spectrum cephalosporins occurred more often in Enterobacter spp. (8.3%, 10/121) than in C. freundii (2.6%, 1/39), S. marcescens (0%, 0/37), or M. morganii (0%, 0/21). Biliary tract infection associated with malignant bile duct invasion was significantly associated with the emergence of resistance to broad-spectrum cephalosporins (P = 0.024 at a significance level of 0.042, by use of the Bonferroni correction). Only 1 of the 14 patients whose isolates developed resistance during antimicrobial therapy died. The emergence of resistance was more frequently associated with broad-spectrum cephalosporins than with the other antimicrobial agents tested, especially in Enterobacter spp. However, the emergence of resistance was associated with a low risk of mortality.
            Article 0 comments Cited 46 times – based on 0 reviews     Review now
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              Porin alterations present in non-carbapenemase-producing Enterobacteriaceae with high and intermediate levels of carbapenem resistance in Chile.

              Aniela Wozniak, Nicolás Villagra, Agustina Undabarrena … (2012)
              The main goal of this work was to identify the mechanisms responsible for carbapenem resistance in 61 Chilean clinical isolates of Enterobacteriaceae (Enterobacter spp., Serratia marcescens, Morganella morganii, Escherichia coli and Klebsiella pneumoniae) with reduced susceptibility to at least one carbapenem (ertapenem, imipenem or meropenem). All of the isolates were analysed for the presence of carbapenemases, extended spectrum β-lactamases (ESBLs), AmpC enzymes and outer-membrane proteins. None of the isolates exhibited carbapenemase activity nor did they have any of the carbapenemase genes that were screened for. Most of the 61 strains produced at least one ESBL and/or one AmpC enzyme and either lost their porins or had altered porins according to sequence analysis. The distribution of ESBLs and AmpC enzymes was different among the species studied. Resistance in K. pneumoniae and E. coli isolates was associated with ESBLs; in M. morganii isolates, resistance was attributed to overexpression of an AmpC enzyme; and in Enterobacter spp. isolates, resistance was associated with both types of enzymes. In K. pneumoniae isolates, porin integrity was more a determinant of carbapenem resistance than the presence of ESBLs, whereas in isolates of Enterobacter spp., M. morganii and S. marcescens, the presence of an overexpressed AmpC enzyme was associated with higher imipenem and meropenem MIC values. Therefore, carbapenem resistance in Chilean isolates is not due to true carbapenemases but rather to a combination of porin loss/alteration and β-lactamase activity. The fact that carbapenemases were not detected in this study is unique, given that many countries in the region have already reported the presence of these enzymes.
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                Author and article information

                Contributors
                Patrick N. A. Harris: +61 7 3346 5476 , p.harris@uq.edu.au
                Anna M. Peri: anninaperi@gmail.com
                Anita M. Pelecanos: Anita.Pelecanos@qimrberghofer.edu.au
                Carly M. Hughes: carly_m_hughes@yahoo.com.au
                David L. Paterson: david.antibiotics@gmail.com
                John K. Ferguson: John.Ferguson@hnehealth.nsw.gov.au
                Journal
                Journal ID (nlm-ta): Antimicrob Resist Infect Control
                Journal ID (iso-abbrev): Antimicrob Resist Infect Control
                Title: Antimicrobial Resistance and Infection Control
                Publisher: BioMed Central (London )
                ISSN (Electronic): 2047-2994
                Publication date (Electronic): 21 January 2017
                Publication date PMC-release: 21 January 2017
                Publication date Collection: 2017
                Volume: 6
                Electronic Location Identifier: 14
                Affiliations
                [1 ]University of Queensland, UQ Centre for Clinical Research, Royal Brisbane and Women’s Hospital, Building 71/918 Royal Brisbane & Women’s Hospital Campus, 4029 Herston, QLD Australia
                [2 ]ISNI 0000 0004 1757 2822, GRID grid.4708.b, Department of Biomedical and Clinical Sciences Luigi Sacco, , University of Milan, ; Milan, Italy
                [3 ]ISNI 0000 0001 2294 1395, GRID grid.1049.c, , QIMR Berghofer Medical Research Institute, ; Herston, QLD Australia
                [4 ]ISNI 0000 0004 0577 6676, GRID grid.414724.0, Pathology North - Hunter, , John Hunter Hospital, ; Newcastle, NSW Australia
                [5 ]ISNI 0000 0000 9320 7537, GRID grid.1003.2, UQ Centre for Clinical Research, Royal Brisbane and Women’s Hospital, QLD, Australia & Wesley Medical Research, , University of Queensland, ; Toowong, QLD Australia
                [6 ]ISNI 0000 0000 8831 109X, GRID grid.266842.c, School of Biomedical Sciences and Pharmacy, , University of Newcastle, ; Newcastle, NSW Australia
                [7 ]ISNI 0000 0004 1936 7371, GRID grid.1020.3, School of Rural Medicine, , University of New England, ; Armidale, NSW Australia
                Article
                Publisher ID: 177
                DOI: 10.1186/s13756-017-0177-0
                PMC ID: 5251334
                PubMed ID: 28127422
                SO-VID: fffd9f40-48e5-49e6-9811-ba4ee41a3f2c
                Copyright © © The Author(s). 2017
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 26 November 2016
                Date accepted : 18 January 2017
                Categories
                Subject: Research
                Custom metadata
                issue-copyright-statement © The Author(s) 2017

                ScienceOpen disciplines: Infectious disease & Microbiology
                Keywords: enterobacter cloacae,enterobacter aerogenes,beta-lactamase,ampc,bacteraemia,outcomes,relapse,treatment
                Data availability:
                ScienceOpen disciplines: Infectious disease & Microbiology
                Keywords: enterobacter cloacae, enterobacter aerogenes, beta-lactamase, ampc, bacteraemia, outcomes, relapse, treatment

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